1887

Abstract

The emergence of Acinetobacter baumannii strains, with broad multidrug-resistance phenotypes and novel virulence factors unique to hypervirulent strains, presents a major threat to human health worldwide. Although a number of studies have described virulence-affecting entities for this organism, very few have identified regulatory elements controlling their expression. Previously, our group has documented the global identification and curation of regulatory RNAs in A. baumannii. As such, in the present study, we detail an extension of this work, the performance of an extensive bioinformatic analysis to identify regulatory proteins in the recently annotated genome of the highly virulent AB5075 strain. In so doing, 243 transcription factors, 14 two-component systems (TCSs), 2 orphan response regulators, 1 hybrid TCS and 5 σ factors were found. A comparison of these elements between AB5075 and other clinical isolates, as well as a laboratory strain, led to the identification of several conserved regulatory elements, whilst at the same time uncovering regulators unique to hypervirulent strains. Lastly, by comparing regulatory elements compiled in this study to genes shown to be essential for AB5075 infection, we were able to highlight elements with a specific importance for pathogenic behaviour. Collectively, our work offers a unique insight into the regulatory network of A. baumannii strains, and provides insight into the evolution of hypervirulent lineages.

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2017-03-23
2019-10-23
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References

  1. Jawad A, Seifert H, Snelling AM, Heritage J, Hawkey PM. Survival of Acinetobacter baumannii on dry surfaces: comparison of outbreak and sporadic isolates. J Clin Microbiol 1998;36:1938–1941[PubMed]
    [Google Scholar]
  2. Wendt C, Dietze B, Dietz E, Rüden H. Survival of Acinetobacter baumannii on dry surfaces. J Clin Microbiol 1997;35:1394–1397[PubMed]
    [Google Scholar]
  3. Tsakiridou E, Makris D, Daniil Z, Manoulakas E, Chatzipantazi V et al. Acinetobacter baumannii infection in prior ICU bed occupants is an independent risk factor for subsequent cases of ventilator-associated pneumonia. Biomed Res Int 2014;2014:193516 [CrossRef]
    [Google Scholar]
  4. Guerrero DM, Perez F, Conger NG, Solomkin JS, Adams MD et al. Acinetobacter baumannii-associated skin and soft tissue infections: recognizing a broadening spectrum of disease. Surg Infect 2010;11:49–57 [CrossRef][PubMed]
    [Google Scholar]
  5. Davis KA, Moran KA, Mcallister CK, Gray PJ. Multidrug-resistant Acinetobacter extremity infections in soldiers. Emerg Infect Dis 2005;11:1218–1224 [CrossRef][PubMed]
    [Google Scholar]
  6. Doyle JS, Buising KL, Thursky KA, Worth LJ, Richards MJ. Epidemiology of infections acquired in intensive care units. Semin Respir Crit Care Med 2011;32:115–138 [CrossRef][PubMed]
    [Google Scholar]
  7. Ramírez MS, Vilacoba E, Stietz MS, Merkier AK, Jeric P et al. Spreading of AbaR-type genomic islands in multidrug resistance Acinetobacter baumannii strains belonging to different clonal complexes. Curr Microbiol 2013;67:9–14 [CrossRef][PubMed]
    [Google Scholar]
  8. Post V, White PA, Hall RM. Evolution of AbaR-type genomic resistance islands in multiply antibiotic-resistant Acinetobacter baumannii. J Antimicrob Chemother 2010;65:1162–1170 [CrossRef][PubMed]
    [Google Scholar]
  9. Adams MD, Chan ER, Molyneaux ND, Bonomo RA. Genomewide analysis of divergence of antibiotic resistance determinants in closely related isolates of Acinetobacter baumannii. Antimicrob Agents Chemother 2010;54:3569–3577 [CrossRef][PubMed]
    [Google Scholar]
  10. Smith MG, Gianoulis TA, Pukatzki S, Mekalanos JJ, Ornston LN et al. New insights into Acinetobacter baumannii pathogenesis revealed by high-density pyrosequencing and transposon mutagenesis. Genes Dev 2007;21:601–614 [CrossRef][PubMed]
    [Google Scholar]
  11. Sahl JW, Johnson JK, Harris AD, Phillippy AM, Hsiao WW et al. Genomic comparison of multi-drug resistant invasive and colonizing Acinetobacter baumannii isolated from diverse human body sites reveals genomic plasticity. BMC Genomics 2011;12:291 [CrossRef][PubMed]
    [Google Scholar]
  12. Gebhardt MJ, Gallagher LA, Jacobson RK, Usacheva EA, Peterson LR et al. Joint transcriptional control of virulence and resistance to antibiotic and environmental stress in Acinetobacter baumannii. MBio 2015;6:e01660-15 [CrossRef][PubMed]
    [Google Scholar]
  13. Zurawski DV, Thompson MG, Mcqueary CN, Matalka MN, Sahl JW et al. Genome sequences of four divergent multidrug-resistant Acinetobacter baumannii strains isolated from patients with sepsis or osteomyelitis. J Bacteriol 2012;194:1619–1620 [CrossRef][PubMed]
    [Google Scholar]
  14. Jacobs AC, Thompson MG, Black CC, Kessler JL, Clark LP et al. AB5075, a highly virulent isolate of Acinetobacter baumannii, as a model strain for the evaluation of pathogenesis and antimicrobial treatments. MBio 2014;5:e01076-14 [CrossRef][PubMed]
    [Google Scholar]
  15. Balleza E, López-Bojorquez LN, Martínez-Antonio A, Resendis-Antonio O, Lozada-Chávez I et al. Regulation by transcription factors in bacteria: beyond description. FEMS Microbiol Rev 2009;33:133–151 [CrossRef][PubMed]
    [Google Scholar]
  16. Mitrophanov AY, Groisman EA. Signal integration in bacterial two-component regulatory systems. Genes Dev 2008;22:2601–2611 [CrossRef][PubMed]
    [Google Scholar]
  17. Feklístov A, Sharon BD, Darst SA, Gross CA. Bacterial sigma factors: a historical, structural, and genomic perspective. Annu Rev Microbiol 2014;68:357–376 [CrossRef][PubMed]
    [Google Scholar]
  18. Yoon EJ, Courvalin P, Grillot-Courvalin C. RND-type efflux pumps in multidrug-resistant clinical isolates of Acinetobacter baumannii: major role for AdeABC overexpression and AdeRS mutations. Antimicrob Agents Chemother 2013;57:2989–2995 [CrossRef][PubMed]
    [Google Scholar]
  19. Coyne S, Rosenfeld N, Lambert T, Courvalin P, Périchon B. Overexpression of resistance-nodulation-cell division pump AdeFGH confers multidrug resistance in Acinetobacter baumannii. Antimicrob Agents Chemother 2010;54:4389–4393 [CrossRef][PubMed]
    [Google Scholar]
  20. Rosenfeld N, Bouchier C, Courvalin P, Périchon B. Expression of the resistance-nodulation-cell division pump AdeIJK in Acinetobacter baumannii is regulated by AdeN, a TetR-type regulator. Antimicrob Agents Chemother 2012;56:2504–2510 [CrossRef][PubMed]
    [Google Scholar]
  21. Daniel C, Haentjens S, Bissinger MC, Courcol RJ. Characterization of the Acinetobacter baumannii Fur regulator: cloning and sequencing of the fur homolog gene. FEMS Microbiol Lett 1999;170:199–209[PubMed]
    [Google Scholar]
  22. Mihara K, Tanabe T, Yamakawa Y, Funahashi T, Nakao H et al. Identification and transcriptional organization of a gene cluster involved in biosynthesis and transport of acinetobactin, a siderophore produced by Acinetobacter baumannii ATCC 19606T. Microbiology 2004;150:2587–2597 [CrossRef][PubMed]
    [Google Scholar]
  23. Srinivasan VB, Vaidyanathan V, Rajamohan G. AbuO, a TolC-like outer membrane protein of Acinetobacter baumannii, is involved in antimicrobial and oxidative stress resistance. Antimicrob Agents Chemother 2015;59:1236–1245 [CrossRef][PubMed]
    [Google Scholar]
  24. Mortensen BL, Rathi S, Chazin WJ, Skaar EP. Acinetobacter baumannii response to host-mediated zinc limitation requires the transcriptional regulator Zur. J Bacteriol 2014;196:2616–2626 [CrossRef][PubMed]
    [Google Scholar]
  25. Tomaras AP, Flagler MJ, Dorsey CW, Gaddy JA, Actis LA. Characterization of a two-component regulatory system from Acinetobacter baumannii that controls biofilm formation and cellular morphology. Microbiology 2008;154:3398–3409 [CrossRef][PubMed]
    [Google Scholar]
  26. Geisinger E, Isberg RR. Antibiotic modulation of capsular exopolysaccharide and virulence in Acinetobacter baumannii. PLoS Pathog 2015;11:e1004691 [CrossRef][PubMed]
    [Google Scholar]
  27. Arroyo LA, Herrera CM, Fernandez L, Hankins JV, Trent MS et al. The pmrCAB operon mediates polymyxin resistance in Acinetobacter baumannii ATCC 17978 and clinical isolates through phosphoethanolamine modification of lipid A. Antimicrob Agents Chemother 2011;55:3743–3751 [CrossRef][PubMed]
    [Google Scholar]
  28. Peleg AY, Adams J, Paterson DL. Tigecycline efflux as a mechanism for nonsusceptibility in Acinetobacter baumannii. Antimicrob Agents Chemother 2007;51:2065–2069 [CrossRef][PubMed]
    [Google Scholar]
  29. Lopes BS, Amyes SG. Insertion sequence disruption of adeR and ciprofloxacin resistance caused by efflux pumps and gyrA and parC mutations in Acinetobacter baumannii. Int J Antimicrob Agents 2013;41:117–121 [CrossRef][PubMed]
    [Google Scholar]
  30. Lin MF, Lin YY, Yeh HW, Lan CY. Role of the BaeSR two-component system in the regulation of Acinetobacter baumannii adeAB genes and its correlation with tigecycline susceptibility. BMC Microbiol 2014;14:119 [CrossRef][PubMed]
    [Google Scholar]
  31. Cerqueira GM, Kostoulias X, Khoo C, Aibinu I, Qu Y et al. A global virulence regulator in Acinetobacter baumannii and its control of the phenylacetic acid catabolic pathway. J Infect Dis 2014;210:46–55 [CrossRef][PubMed]
    [Google Scholar]
  32. Weiss A, Broach WH, Lee MC, Shaw LN. Towards the complete small RNome of Acinetobacter baumannii. Microb Genom 2016;2::doi: 10.1099/mgen.0.000045
    [Google Scholar]
  33. Pérez-Rueda E, Tenorio-Salgado S, Huerta-Saquero A, Balderas-Martínez YI, Moreno-Hagelsieb G. The functional landscape bound to the transcription factors of Escherichia coli K-12. Comput Biol Chem 2015;58:93–103 [CrossRef][PubMed]
    [Google Scholar]
  34. Moreno-Campuzano S, Janga SC, Pérez-Rueda E. Identification and analysis of DNA-binding transcription factors in Bacillus subtilis and other firmicutes - a genomic approach. BMC Genomics 2006;7:147 [CrossRef][PubMed]
    [Google Scholar]
  35. Ibarra JA, Pérez-Rueda E, Carroll RK, Shaw LN. Global analysis of transcriptional regulators in Staphylococcus aureus. BMC Genomics 2013;14:126 [CrossRef][PubMed]
    [Google Scholar]
  36. Diancourt L, Passet V, Nemec A, Dijkshoorn L, Brisse S. The population structure of Acinetobacter baumannii: expanding multiresistant clones from an ancestral susceptible genetic pool. PLoS One 2010;5:e10034 [CrossRef][PubMed]
    [Google Scholar]
  37. Gallagher LA, Ramage E, Weiss EJ, Radey M, Hayden HS et al. Resources for genetic and genomic analysis of emerging pathogen Acinetobacter baumannii. J Bacteriol 2015;197:2027–2035 [CrossRef][PubMed]
    [Google Scholar]
  38. Jones CL, Clancy M, Honnold C, Singh S, Snesrud E et al. Fatal outbreak of an emerging clone of extensively drug-resistant Acinetobacter baumannii with enhanced virulence. Clin Infect Dis 2015;61:145–154 [CrossRef][PubMed]
    [Google Scholar]
  39. Messer W, Weigel C. DnaA as a transcription regulator. Methods Enzymol 2003;370:338–349 [CrossRef][PubMed]
    [Google Scholar]
  40. Bogan JA, Helmstetter CE. mioC transcription, initiation of replication, and the eclipse in Escherichia coli. J Bacteriol 1996;178:3201–3206 [CrossRef][PubMed]
    [Google Scholar]
  41. Scholz A, Stahl J, de Berardinis V, Müller V, Averhoff B. Osmotic stress response in Acinetobacter baylyi : identification of a glycine-betaine biosynthesis pathway and regulation of osmoadaptive choline uptake and glycine-betaine synthesis through a choline-responsive BetI repressor. Environ Microbiol Rep 2016;8:316–322 [CrossRef]
    [Google Scholar]
  42. Lee EC, Hales LM, Gumport RI, Gardner JF. The isolation and characterization of mutants of the integration host factor (IHF) of Escherichia coli with altered, expanded DNA-binding specificities. EMBO J 1992;11:305–313[PubMed]
    [Google Scholar]
  43. Eisenstein BI, Sweet DS, Vaughn V, Friedman DI. Integration host factor is required for the DNA inversion that controls phase variation in Escherichia coli. Proc Natl Acad Sci USA 1987;84:6506–6510 [CrossRef][PubMed]
    [Google Scholar]
  44. West SE, Sample AK, Runyen-Janecky LJ. The vfr gene product, required for Pseudomonas aeruginosa exotoxin A and protease production, belongs to the cyclic AMP receptor protein family. J Bacteriol 1994;176:7532–7542 [CrossRef][PubMed]
    [Google Scholar]
  45. González-Gil G, Bringmann P, Kahmann R. FIS is a regulator of metabolism in Escherichia coli. Mol Microbiol 1996;22:21–29 [CrossRef][PubMed]
    [Google Scholar]
  46. Schneider R, Travers A, Muskhelishvili G. The expression of the Escherichia coli fis gene is strongly dependent on the superhelical density of DNA. Mol Microbiol 2000;38:167–175 [CrossRef][PubMed]
    [Google Scholar]
  47. Popp R, Kohl T, Patz P, Trautwein G, Gerischer U. Differential DNA binding of transcriptional regulator PcaU from Acinetobacter sp. strain ADP1. J Bacteriol 2002;184:1988–1997 [CrossRef][PubMed]
    [Google Scholar]
  48. Trautwein G, Gerischer U. Effects exerted by transcriptional regulator PcaU from Acinetobacter sp. strain ADP1. J Bacteriol 2001;183:873–881 [CrossRef][PubMed]
    [Google Scholar]
  49. Haines S, Arnaud-Barbe N, Poncet D, Reverchon S, Wawrzyniak J et al. IscR regulates synthesis of colonization factor antigen I fimbriae in response to iron starvation in enterotoxigenic Escherichia coli. J Bacteriol 2015;197:2896–2907 [CrossRef][PubMed]
    [Google Scholar]
  50. Adams MD, Goglin K, Molyneaux N, Hujer KM, Lavender H et al. Comparative genome sequence analysis of multidrug-resistant Acinetobacter baumannii. J Bacteriol 2008;190:8053–8064 [CrossRef][PubMed]
    [Google Scholar]
  51. Poirel L, Menuteau O, Agoli N, Cattoen C, Nordmann P. Outbreak of extended-spectrum beta-lactamase VEB-1-producing isolates of Acinetobacter baumannii in a French hospital. J Clin Microbiol 2003;41:3542–3547 [CrossRef][PubMed]
    [Google Scholar]
  52. Iacono M, Villa L, Fortini D, Bordoni R, Imperi F et al. Whole-genome pyrosequencing of an epidemic multidrug-resistant Acinetobacter baumannii strain belonging to the European clone II group. Antimicrob Agents Chemother 2008;52:2616–2625 [CrossRef][PubMed]
    [Google Scholar]
  53. Whitchurch CB, Alm RA, Mattick JS. The alginate regulator AlgR and an associated sensor FimS are required for twitching motility in Pseudomonas aeruginosa. Proc Natl Acad Sci USA 1996;93:9839–9843 [CrossRef][PubMed]
    [Google Scholar]
  54. Torrents E, Grinberg I, Gorovitz-Harris B, Lundström H, Borovok I et al. NrdR controls differential expression of the Escherichia coli ribonucleotide reductase genes. J Bacteriol 2007;189:5012–5021 [CrossRef][PubMed]
    [Google Scholar]
  55. Espin G, Alvarez-Morales A, Cannon F, Dixon R, Merrick M. Cloning of the glnA, ntrB and ntrC genes of Klebsiella pneumoniae and studies of their role in regulation of the nitrogen fixation (nif) gene cluster. Mol Gen Genet 1982;186:518–524 [CrossRef][PubMed]
    [Google Scholar]
  56. Huillet E, Velge P, Vallaeys T, Pardon P. LadR, a new PadR-related transcriptional regulator from Listeria monocytogenes, negatively regulates the expression of the multidrug efflux pump MdrL. FEMS Microbiol Lett 2006;254:87–94 [CrossRef][PubMed]
    [Google Scholar]
  57. Fibriansah G, Kovács ÁT, Pool TJ, Boonstra M, Kuipers OP et al. Crystal structures of two transcriptional regulators from Bacillus cereus define the conserved structural features of a PadR subfamily. PLoS One 2012;7:e48015 [CrossRef][PubMed]
    [Google Scholar]
  58. Ueguchi C, Kakeda M, Mizuno T. Autoregulatory expression of the Escherichia coli hns gene encoding a nucleoid protein: H-Ns functions as a repressor of its own transcription. Mol Gen Genet 1993;236:171–178 [CrossRef][PubMed]
    [Google Scholar]
  59. Robbe-Saule V, Schaeffer F, Kowarz L, Norel F. Relationships between H-NS, sigma S, SpvR and growth phase in the control of spvR, the regulatory gene of the Salmonella plasmid virulence operon. Mol Gen Genet 1997;256:333–347 [CrossRef][PubMed]
    [Google Scholar]
  60. Yurimoto H, Hirai R, Matsuno N, Yasueda H, Kato N et al. HxlR, a member of the DUF24 protein family, is a DNA-binding protein that acts as a positive regulator of the formaldehyde-inducible hxlAB operon in Bacillus subtilis. Mol Microbiol 2005;57:511–519 [CrossRef][PubMed]
    [Google Scholar]
  61. Wang X, Kim Y, Wood TK. Control and benefits of CP4-57 prophage excision in Escherichia coli biofilms. ISME J 2009;3:1164–1179 [CrossRef][PubMed]
    [Google Scholar]
  62. Antunes LC, Imperi F, Carattoli A, Visca P. Deciphering the multifactorial nature of Acinetobacter baumannii pathogenicity. PLoS One 2011;6:e22674 [CrossRef][PubMed]
    [Google Scholar]
  63. Peleg AY, Jara S, Monga D, Eliopoulos GM, Moellering RC et al. Galleria mellonella as a model system to study Acinetobacter baumannii pathogenesis and therapeutics. Antimicrob Agents Chemother 2009;53:2605–2609 [CrossRef][PubMed]
    [Google Scholar]
  64. De Léséleuc L, Harris G, Kuolee R, Xu HH, Chen W. Serum resistance, gallium nitrate tolerance and extrapulmonary dissemination are linked to heme consumption in a bacteremic strain of Acinetobacter baumannii. Int J Med Microbiol 2014;304:360–369 [CrossRef][PubMed]
    [Google Scholar]
  65. Mcconnell MJ, Actis L, Pachón J. Acinetobacter baumannii: human infections, factors contributing to pathogenesis and animal models. FEMS Microbiol Rev 2013;37:130–155 [CrossRef][PubMed]
    [Google Scholar]
  66. Krell T, Lacal J, Busch A, Silva-Jiménez H, Guazzaroni ME et al. Bacterial sensor kinases: diversity in the recognition of environmental signals. Annu Rev Microbiol 2010;64:539–559 [CrossRef][PubMed]
    [Google Scholar]
  67. Marchand I, Damier-Piolle L, Courvalin P, Lambert T. Expression of the RND-type efflux pump AdeABC in Acinetobacter baumannii is regulated by the AdeRS two-component system. Antimicrob Agents Chemother 2004;48:3298–3304 [CrossRef][PubMed]
    [Google Scholar]
  68. Jin S, Ishimoto KS, Lory S. PilR, a transcriptional regulator of piliation in Pseudomonas aeruginosa, binds to a cis-acting sequence upstream of the pilin gene promoter. Mol Microbiol 1994;14:1049–1057 [CrossRef][PubMed]
    [Google Scholar]
  69. Eijkelkamp BA, Stroeher UH, Hassan KA, Papadimitrious MS, Paulsen IT et al. Adherence and motility characteristics of clinical Acinetobacter baumannii isolates. FEMS Microbiol Lett 2011;323:44–51 [CrossRef][PubMed]
    [Google Scholar]
  70. Clemmer KM, Bonomo RA, Rather PN. Genetic analysis of surface motility in Acinetobacter baumannii. Microbiology 2011;157:2534–2544 [CrossRef][PubMed]
    [Google Scholar]
  71. Jones AL, Deshazer D, Woods DE. Identification and characterization of a two-component regulatory system involved in invasion of eukaryotic cells and heavy-metal resistance in Burkholderia pseudomallei. Infect Immun 1997;65:4972–4977[PubMed]
    [Google Scholar]
  72. Gross CA, Grossman AD, Liebke H, Walter W, Burgess RR. Effects of the mutant sigma allele rpoD800 on the synthesis of specific macromolecular components of the Escherichia coli K12 cell. J Mol Biol 1984;172:283–300 [CrossRef][PubMed]
    [Google Scholar]
  73. Grossman AD, Zhou YN, Gross C, Heilig J, Christie GE et al. Mutations in the rpoH (htpR) gene of Escherichia coli K-12 phenotypically suppress a temperature-sensitive mutant defective in the sigma 70 subunit of RNA polymerase. J Bacteriol 1985;161:939–943[PubMed]
    [Google Scholar]
  74. Siegele DA, Hu JC, Walter WA, Gross CA. Altered promoter recognition by mutant forms of the sigma 70 subunit of Escherichia coli RNA polymerase. J Mol Biol 1989;206:591–603 [CrossRef][PubMed]
    [Google Scholar]
  75. Rouvière PE, de Las Peñas A, Mecsas J, Lu CZ, Rudd KE et al. rpoE, the gene encoding the second heat-shock sigma factor, sigma E, in Escherichia coli. EMBO J 1995;14:1032–1042[PubMed]
    [Google Scholar]
  76. Taylor M, Butler R, Chambers S, Casimiro M, Badii F et al. The RpoN-box motif of the RNA polymerase sigma factor sigma N plays a role in promoter recognition. Mol Microbiol 1996;22:1045–1054 [CrossRef][PubMed]
    [Google Scholar]
  77. Mahren S, Braun V. The FecI extracytoplasmic-function sigma factor of Escherichia coli interacts with the β' subunit of RNA polymerase. J Bacteriol 2003;185:1796–1802 [CrossRef][PubMed]
    [Google Scholar]
  78. Potvin E, Sanschagrin F, Levesque RC. Sigma factors in Pseudomonas aeruginosa. FEMS Microbiol Rev 2008;32:38–55 [CrossRef][PubMed]
    [Google Scholar]
  79. Hirschman J, Wong PK, Sei K, Keener J, Kustu S. Products of nitrogen regulatory genes ntrA and ntrC of enteric bacteria activate glnA transcription in vitro: evidence that the ntrA product is a sigma factor. Proc Natl Acad Sci USA 1985;82:7525–7529 [CrossRef][PubMed]
    [Google Scholar]
  80. Arnold HM, Sawyer AM, Kollef MH. Use of adjunctive aerosolized antimicrobial therapy in the treatment of Pseudomonas aeruginosa and Acinetobacter baumannii ventilator-associated pneumonia. Respir Care 2012;57:1226–1233 [CrossRef][PubMed]
    [Google Scholar]
  81. Mccarty JS, Rüdiger S, Schönfeld HJ, Schneider-Mergener J, Nakahigashi K et al. Regulatory region C of the E. coli heat shock transcription factor, sigma32, constitutes a DnaK binding site and is conserved among eubacteria. J Mol Biol 1996;256:829–837 [CrossRef][PubMed]
    [Google Scholar]
  82. Hsieh M, Gralla JD. Analysis of the N-terminal leucine heptad and hexad repeats of sigma 54. J Mol Biol 1994;239:15–24 [CrossRef][PubMed]
    [Google Scholar]
  83. Doucleff M, Malak LT, Pelton JG, Wemmer DE. The C-terminal RpoN domain of sigma54 forms an unpredicted helix-turn-helix motif similar to domains of sigma70. J Biol Chem 2005;280:41530–41536 [CrossRef][PubMed]
    [Google Scholar]
  84. Mahren S, Enz S, Braun V. Functional interaction of region 4 of the extracytoplasmic function sigma factor FecI with the cytoplasmic portion of the FecR transmembrane protein of the Escherichia coli ferric citrate transport system. J Bacteriol 2002;184:3704–3711 [CrossRef][PubMed]
    [Google Scholar]
  85. Campbell EA, Tupy JL, Gruber TM, Wang S, Sharp MM et al. Crystal structure of Escherichia coli sigmaE with the cytoplasmic domain of its anti-sigma RseA. Mol Cell 2003;11:1067–1078 [CrossRef][PubMed]
    [Google Scholar]
  86. Tam C, Collinet B, Lau G, Raina S, Missiakas D. Interaction of the conserved region 4.2 of sigma(E) with the RseA anti-sigma factor. J Biol Chem 2002;277:27282–27287 [CrossRef][PubMed]
    [Google Scholar]
  87. Lane WJ, Darst SA. The structural basis for promoter -35 element recognition by the group IV sigma factors. PLoS Biol 2006;4:e269 [CrossRef][PubMed]
    [Google Scholar]
  88. Braun V, Mahren S, Ogierman M. Regulation of the FecI-type ECF sigma factor by transmembrane signalling. Curr Opin Microbiol 2003;6:173–180 [CrossRef][PubMed]
    [Google Scholar]
  89. Schmitt MP. Transcription of the Corynebacterium diphtheriae hmuO gene is regulated by iron and heme. Infect Immun 1997;65:4634–4641[PubMed]
    [Google Scholar]
  90. Zhu W, Hunt DJ, Richardson AR, Stojiljkovic I. Use of heme compounds as iron sources by pathogenic neisseriae requires the product of the hemO gene. J Bacteriol 2000;182:439–447 [CrossRef][PubMed]
    [Google Scholar]
  91. Ratliff M, Zhu W, Deshmukh R, Wilks A, Stojiljkovic I. Homologues of neisserial heme oxygenase in gram-negative bacteria: degradation of heme by the product of the pigA gene of Pseudomonas aeruginosa. J Bacteriol 2001;183:6394–6403 [CrossRef][PubMed]
    [Google Scholar]
  92. Carroll RK, Weiss A, Broach WH, Wiemels RE, Mogen AB et al. Genome-wide annotation, identification, and global transcriptomic analysis of regulatory or small RNA gene expression in Staphylococcus aureus. MBio 2016;7:e01990-15 [CrossRef][PubMed]
    [Google Scholar]
  93. Takinowaki H, Matsuda Y, Yoshida T, Kobayashi Y, Ohkubo T. The solution structure of the methylated form of the N-terminal 16-kDa domain of Escherichia coli Ada protein. Protein Sci 2006;15:487–497 [CrossRef][PubMed]
    [Google Scholar]
  94. Carlin A, Shi W, Dey S, Rosen BP. The ars operon of Escherichia coli confers arsenical and antimonial resistance. J Bacteriol 1995;177:981–986 [CrossRef][PubMed]
    [Google Scholar]
  95. Xu C, Shi W, Rosen BP. The chromosomal arsR gene of Escherichia coli encodes a trans-acting metalloregulatory protein. J Biol Chem 1996;271:2427–2432 [CrossRef][PubMed]
    [Google Scholar]
  96. Giangrossi M, Giuliodori AM, Gualerzi CO, Pon CL. Selective expression of the beta-subunit of nucleoid-associated protein HU during cold shock in Escherichia coli. Mol Microbiol 2002;44:205–216 [CrossRef][PubMed]
    [Google Scholar]
  97. Fuchs EL, Brutinel ED, Jones AK, Fulcher NB, Urbanowski ML et al. The Pseudomonas aeruginosa vfr regulator controls global virulence factor expression through cyclic AMP-dependent and -independent mechanisms. J Bacteriol 2010;192:3553–3564 [CrossRef][PubMed]
    [Google Scholar]
  98. Kücherer C, Lother H, Kölling R, Schauzu MA, Messer W. Regulation of transcription of the chromosomal dnaA gene of Escherichia coli. Mol Gen Genet 1986;205:115–121 [CrossRef][PubMed]
    [Google Scholar]
  99. Gao YG, Suzuki H, Itou H, Zhou Y, Tanaka Y et al. Structural and functional characterization of the LldR from Corynebacterium glutamicum: a transcriptional repressor involved in L-lactate and sugar utilization. Nucleic Acids Res 2008;36:7110–7123 [CrossRef][PubMed]
    [Google Scholar]
  100. Aguilera L, Campos E, Giménez R, Badía J, Aguilar J et al. Dual role of LldR in regulation of the lldPRD operon, involved in L-lactate metabolism in Escherichia coli. J Bacteriol 2008;190:2997–3005 [CrossRef][PubMed]
    [Google Scholar]
  101. Morawski B, Segura A, Ornston LN. Repression of Acinetobacter vanillate demethylase synthesis by VanR, a member of the GntR family of transcriptional regulators. FEMS Microbiol Lett 2000;187:65–68 [CrossRef][PubMed]
    [Google Scholar]
  102. Sieira R, Arocena GM, Bukata L, Comerci DJ, Ugalde RA. Metabolic control of virulence genes in Brucella abortus: hutc coordinates virB expression and the histidine utilization pathway by direct binding to both promoters. J Bacteriol 2010;192:217–224 [CrossRef][PubMed]
    [Google Scholar]
  103. Kok RG, D'Argenio DA, Ornston LN. Mutation analysis of PobR and PcaU, closely related transcriptional activators in Acinetobacter. J Bacteriol 1998;180:5058–5069[PubMed]
    [Google Scholar]
  104. Arias-Barrau E, Olivera ER, Luengo JM, Fernández C, Galán B et al. The homogentisate pathway: a central catabolic pathway involved in the degradation of L-phenylalanine, L-tyrosine, and 3-hydroxyphenylacetate in Pseudomonas putida. J Bacteriol 2004;186:5062–5077 [CrossRef][PubMed]
    [Google Scholar]
  105. Yeung AT, Torfs EC, Jamshidi F, Bains M, Wiegand I et al. Swarming of Pseudomonas aeruginosa is controlled by a broad spectrum of transcriptional regulators, including MetR. J Bacteriol 2009;191:5592–5602 [CrossRef][PubMed]
    [Google Scholar]
  106. Chugani SA, Parsek MR, Chakrabarty AM. Transcriptional repression mediated by LysR-type regulator CatR bound at multiple binding sites.. J Bacteriol 1998;180:2367–2372[PubMed]
    [Google Scholar]
  107. Craven SH, Ezezika OC, Haddad S, Hall RA, Momany C et al. Inducer responses of BenM, a LysR-type transcriptional regulator from Acinetobacter baylyi ADP1. Mol Microbiol 2009;72:881–894 [CrossRef][PubMed]
    [Google Scholar]
  108. Collier LS, Gaines GL, Neidle EL. Regulation of benzoate degradation in Acinetobacter sp. strain ADP1 by BenM, a LysR-type transcriptional activator.. J Bacteriol 1998;180:2493–2501[PubMed]
    [Google Scholar]
  109. Marbaniang CN, Gowrishankar J. Role of ArgP (IciA) in lysine-mediated repression in Escherichia coli. J Bacteriol 2011;193:5985–5996 [CrossRef][PubMed]
    [Google Scholar]
  110. Díaz E, Ferrández A, García JL. Characterization of the hca cluster encoding the dioxygenolytic pathway for initial catabolism of 3-phenylpropionic acid in Escherichia coli K-12. J Bacteriol 1998;180:2915–2923[PubMed]
    [Google Scholar]
  111. van der Ploeg JR, Eichhorn E, Leisinger T. Sulfonate-sulfur metabolism and its regulation in Escherichia coli. Arch Microbiol 2001;176:1–8 [CrossRef][PubMed]
    [Google Scholar]
  112. Kertesz MA. Riding the sulfur cycle – metabolism of sulfonates and sulfate esters in gram-negative Bacteria.. FEMS Microbiol Rev 2000;24:135–175[PubMed]
    [Google Scholar]
  113. Stec E, Witkowska-Zimny M, Hryniewicz MM, Neumann P, Wilkinson AJ et al. Structural basis of the sulphate starvation response in E. coli: crystal structure and mutational analysis of the cofactor-binding domain of the cbl transcriptional regulator. J Mol Biol 2006;364:309–322 [CrossRef][PubMed]
    [Google Scholar]
  114. Graveline R, Garneau P, Martin C, Mourez M, Hancock MA et al. Leucine-responsive regulatory protein lrp and PapI homologues influence phase variation of CS31A fimbriae. J Bacteriol 2014;196:2944–2953 [CrossRef][PubMed]
    [Google Scholar]
  115. Stoyanov JV, Hobman JL, Brown NL. CueR (YbbI) of Escherichia coli is a MerR family regulator controlling expression of the copper exporter CopA. Mol Microbiol 2001;39:502–512 [CrossRef][PubMed]
    [Google Scholar]
  116. Kirby JE, Trempy JE, Gottesman S. Excision of a P4-like cryptic prophage leads to alp protease expression in Escherichia coli. J Bacteriol 1994;176:2068–2081 [CrossRef][PubMed]
    [Google Scholar]
  117. Brocklehurst KR, Megit SJ, Morby AP. Characterisation of CadR from Pseudomonas aeruginosa: a cd(II)-responsive MerR homologue. Biochem Biophys Res Commun 2003;308:234–239 [CrossRef][PubMed]
    [Google Scholar]
  118. Hakkila KM, Nikander PA, Junttila SM, Lamminmäki UJ, Virta MP. Cd-specific mutants of mercury-sensing regulatory protein MerR, generated by directed evolution. Appl Environ Microbiol 2011;77:6215–6224 [CrossRef][PubMed]
    [Google Scholar]
  119. Streicher SL, Shanmugam KT, Ausubel F, Morandi C, Goldberg RB. Regulation of nitrogen fixation in Klebsiella pneumoniae: evidence for a role of glutamine synthetase as a regulator of nitrogenase synthesis.. J Bacteriol 1974;120:815–821[PubMed]
    [Google Scholar]
  120. Srinivasan VB, Venkataramaiah M, Mondal A, Vaidyanathan V, Govil T et al. Functional characterization of a novel outer membrane porin KpnO, regulated by PhoBR two-component system in Klebsiella pneumoniae NTUH-K2044. PLoS One 2012;7:e41505 [CrossRef][PubMed]
    [Google Scholar]
  121. Forst S, Delgado J, Inouye M. Phosphorylation of OmpR by the osmosensor EnvZ modulates expression of the ompF and ompC genes in Escherichia coli. Proc Natl Acad Sci USA 1989;86:6052–6056 [CrossRef][PubMed]
    [Google Scholar]
  122. Delgado J, Forst S, Harlocker S, Inouye M. Identification of a phosphorylation site and functional analysis of conserved aspartic acid residues of OmpR, a transcriptional activator for ompF and ompC in Escherichia coli. Mol Microbiol 1993;10:1037–1047 [CrossRef][PubMed]
    [Google Scholar]
  123. Nakashima K, Sugiura A, Kanamaru K, Mizuno T. Signal transduction between the two regulatory components involved in the regulation of the kdpABC operon in Escherichia coli: phosphorylation-dependent functioning of the positive regulator, KdpE. Mol Microbiol 1993;7:109–116 [CrossRef][PubMed]
    [Google Scholar]
  124. Munson GP, Lam DL, Outten FW, O'Halloran TV. Identification of a copper-responsive two-component system on the chromosome of Escherichia coli K-12. J Bacteriol 2000;182:5864–5871 [CrossRef][PubMed]
    [Google Scholar]
  125. Schelder S, Zaade D, Litsanov B, Bott M, Brocker M. The two-component signal transduction system CopRS of Corynebacterium glutamicum is required for adaptation to copper-excess stress. PLoS One 2011;6:e22143 [CrossRef][PubMed]
    [Google Scholar]
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